THE VELIGER © CMS, Inc., 1998 The Veliger 41(3):239-242 (July I, 1998)

Distribution and Reproductive Biology of Sepietta neglecta (Naef, 1916) (Cephalopoda: Sepioidea) in the North (Eastern Mediterranean) EUGENIA LEFKADITOU National Centre for Marine Research, Athens, Greece

AND PANAYOTIS KASPIRIS Zoological Laboratory, University of Patras, Patras, Greece

Abstract. Sepietta neglecta (Naef, 1916) is the most rarely caught of the Sepietta (). Its presence in the North Aegean Sea (Eastern Mediterranean) is recorded for the first time, on the basis of 56 specimens, collected at depths from 24 to 262 m, during six seasonal trawl surveys carried out from September 1992 to December 1992. Specimens were dissected, weighed, and assigned a maturity stage. The weight-length relationship was found to be allometric. Mature individuals were caught during all six cruises. In mature males, from 150 to 240 spermatophores were counted, whereas in females, up to 127 oocytes were counted of which only a fraction (6-36%) were in the last stage of development. The ovaries of mature females contained oocytes at three vitellogenetic stages: primary oogonia, maturing oocytes, and smooth ripe oocytes ready to be released. The diameter of ripe occytes, in the major axis, ranged from 1.4 to 2.8 mm.

INT RODUCTION information on length-weight relationships, maturity stages, and oocyte size frequencies in mature females. Sepietta neglecta (Naef, 1916) is a small, nectobenthic species with a maximum mantle length of about 30 mm. MATERIALS AND METHODS It is found in the and on the coasts of the Eastern Atlantic from the southern coasts of Norway Fifty-six specimens of Sepietta neglecta were caught (Wirz, 1958) to Morocco (Guerra, 1992). Although it was from trawlable bottoms in the North Aegean Sea (Figure 1) during six seasonal cruises in 1992-1993. A commer­ described by Naef as early as 1916, it is very rarely cial trawler of 115 tons gross tonnage, equipped with twin caught, in contrast to the other two species of the genus 250 Hp engines, echosounder, radar, and plotter, was Sepietta (S. oweniana [d'Orbigny, 1840] and S. obscura hired. The trawl used was a nylon net with a cod-end [Naef, 1916]). Its presence in the Eastern Mediterranean mesh of 16 mm from knot to knot. The bottom area in­ (east of 23°E) was doubtful (Digby, 1949) until 1972 vestigated was subdivided into four depth strata: 0-50 m, when one male specimen was identified by G. Ruby & J. 50-100 m, 100-200 m, 200-500 m; and the sampling Knudsen, in Cyprus waters. More recently, it was record­ was based on random-stratified design. The minimum and ed in the (Katagan et al., 1993). The maximum depths trawled were 16 m and 416 m, respec­ present records represent the first occurrence of Sepietta tively. For each trawl survey, 65 hauls, ranging from 45 neglecta in Greek waters. Most of the published records min to 60 min in duration, were performed. of Sepietta neglecta concern males, perhaps because of The specimens of Sepietta neglecta, together with other the great resemblance of females to those of Sepietta ow­ sepiolids found during the surveys, were preserved in 5% eniana (Naef, 1923), which does not ensure the identifi­ formalin. They were identified in the laboratory under a cation of the species unless individuals of both sexes are dissecting microscope, according to the suggestions of found. Very little information on the biology of this spe­ Naef (1923), i.e., mainly by observing the hectocotylized cies is available in the literature. Its embryonic and post­ arm of the males and, for the females, by comparing the embryonic development to a final mantle length of 15 tentacle and tentacular club sizes with those of equally mm has been studied by Boletzky et al. (1971) by rearing large , which have longer and more ro­ in the aquarium, from eggs collected from bi­ bust tentacles. valve shells trawled off Banyuls-sur-Mer, France (West­ For 48 specimens, dorsal mantle length (DML, mm) ern Mediterranean). The present report contributes to the and weight (gr) were measured; sex and stage of maturity knowledge of the biology of this species by giving some of the gonads (Lipinski, 1979) were assessed. Oocytes Page 240 The Veliger, Vol. 41, No. 3

'- ,r ALBANIA DStageI DStageII D.Stage111 r 20 Dec. 1992 ... ML= 16 mm I 127

'·

40 March 1993 30 I ML • 18 mm " n = 88 20 /_)''···· 10 --� �:}t ,- March 1993 20 ML= 16 mm n = 85 10

June 1993 20 ML= 19 mm Figure n = 135 10 Sampling areas in the North Aegean Sea. A: Thermaikos Gulf; B: Toroneos Gulf; C: Strymonikos Gulf; D: Thracian Sea. .,o Sep. 1993 >, 20 u ML= 18 mm c: Q) n = 103 and spermatophores were counted in 10 mature females :::, 10 and eight males, respectively. Development of the oo­ er ~ cytes of Sepietta neglecta was divided into three stages: lL (I) primary oogonia, (II) maturing oocytes, reticulated by Sep. 1993 invading follicular epithelium, and (III) smooth ripe oo­ 20 � ML= 15 mm n = 100 cytes ready to be released. Ooocyte lengths (longest di­ 10 mension) were measured for each stage, to the nearest 0.01 mm with an ocular micrometer in a stereoscope. 30 Sep. 1993 ML= 18 mm RESULTS 20 n = 102 The 48 specimens examined are listed in Table 1, indi­ 10 cating geographical zone, date of capture, depth of the station, dorsal mantle length and weight of the individu­ 30 Sep. 1993 als, and maturity stage of their gonads. ML= 16 mm 20 n = 73 Sepietta neglecta was found in all the subareas on sand-muddy bottoms, sometimes covered by Crinoidea, 10 and at depths ranging from 24 m to 262 m. Together with Sep. 1993 this sepiolid, other were found that have a 20 ML= 19 mm wide bathymetrical distribution, like Sepietta oweniana, n = 125 Sepiola rondeleti (Leach, 1817), Rondeletiola minor 10 (Waef, 1912), Alloteuthis media (Linnaeus, 1758), Illex coindetii (Verany, 1839), Eledone cirrosa (Lamarck, 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 1.8 2.0 2.2 2.4 2.6 2.8 3.0 3.2 1798), Sepia orbignyana (Ferussac, 1826), and Sepia ele­ Oocyte diameter ( mm ) gans (Blainville, 1827). Loligo vulgaris (Lamarck, 1798), Octopus vulgaris (Cuvier, 1797), and Eledone moschata Figure 2 (Lamarck, 1798) were also found together with Sepietta Frequency distribution of oocyte diameter (longest dimension) of neglecta in shallower stations. three vitellogenic oocyte stages in ovaries of mature (stage IV� Dorsal mantle lengths ranged from 12 mm to 23 mm V) Sepietta neglecta collected seasonally in the North Aegean for females and from 13 mm to 23 mm for males (fixed Sea. Each panel represents the ovary from one female. specimens). Mature individuals were caught throughout the year. Minimum spawning sizes were 16 mm DML in the male and 15 mm DML in the female. In mature males E. Lefkaditou & P. Kaspiris, 1998 Page 241

Table 1 List of specimens of Sepietta neglecta caught during six trawl surveys carried out in the North Aegean sea from 1992 to 1993, with indication of fishing zone, depth, individual size (in mm DML), weight (in gr) and maturity stage in both females and males. A = Thermaikos Gulf; B = Toroneos Gulf; C = Strymonikos Gulf; D = Thracian Sea.

Females Males DML Weight Maturity DML Weight Maturity Date Depth (m) Zone (mm) (gr) stage (mm) (gr) stage 29 Aug. 92 66 A 15.5 2.9 III 19.4 2.4 v 17.5 1.5 v 07 Dec. 92 73 c 18.0 3.5 VI 13.0 1.5 IV 18.8 3.8 v 18.0 2.8 IV 08 Dec. 92 115 c 16.7 2.0 IV 16.0 2.7 v 18.9 2.7 v 18.5 2.4 v 08 Mar. 93 262 B 18.0 2.2 v 16.0 2.4 IV 09 Mar. 93 167 B 13.0 1.5 IV 18.0 2.3 v 15.0 2.4 IV 21.0 2.7 v 12 Mar. 93 115 c 22.1 2.8 v 23.0 3.6 v 16.0 1.8 v 17.0 2.6 IV 19.0 2.8 v 14 Mar. 93 136 c 17.4 2.1 v 15.0 1.7 II 13.0 1.1 III 12.0 1.3 IV 04 Jun. 93 102 A 19.0 2.4 III 05 Jun. 93 71 A 21.0 3.5 v 15.0 1.9 II 18.0 1.8 18.0 2.9 04 Sep. 93 229 A 15.0 1.7 v 14.0 1.7 18.0 2.1 IV 15.0 1.5 II 17.0 2.1 17.0 2.3 IV 13.0 1.2 08 Sep. 93 79 c 16.0 2.1 IV 15.0 1.6 IV 19.0 1.9 v 23.0 3.4 v 17.0 1.9 v 18.0 2.7 v 17.4 2.5 v 16.3 2.1 v 12 Sep. 93 80 D 19.0 2.3 IV 17 Dec. 93 24 D 22.0 3.2

(Lipinski stage IV), from 150 to 240 spermatophores sexes given the small number of individuals available. were found, the maximum length of which was 5.9 mm. The resulting power function was: Maximum oocyte count in the ovaries of 10 mature (Lip­ 1528 2 inski stages IV, V) females was 127. However, only a W = 0.000285 * ML r = 0.614 fraction of the ova, ranging from 6% to 36%, were in the from which the allometric nature of the growth of Se­ last stage of development. The ovaries contained oocytes pietta neglecta can be recognized. at all three stages. Size frequencies of the oocytes in nine mature females are presented in Figure 2. The maximum DISCUSSION diameter of oocytes ranged from 0.1 to 1.2 mm in stage I, from 1.2 to 2.75 mm in the stage II, and from 1.4 to The records of Sepietta neglecta in the North Aegean Sea 2.83 mm for the smooth oocytes at stage III. confirm the wide distribution of the species in the Med­ A least square regression equation was calculated from iterranean Sea. The bathymetric distribution in the North the logarithmically transformed dorsal mantle length Aegean Sea does not seem to be correlated with sex, as (DML, mm) and body weight (W, gr) data, pooling both far as our data suggest. The species was found from in- Page 242 The Veliger, Vol. 41, No. 3 fralittoral to bathyal grounds, as was expected from other des reunions. Commission internationale pour 1' Exploration records in Cyprus waters: 135 m (Ruby & Knudsen, Scientifique de la Mer Mediterranee, Vol. 28(5):281. 1972), in the Gulf of Cadiz: 70-475 m (Guerra, 1982), BOLETZKY, S. V., M. V. V. BOLETZKY, D. FROSCH & V. GATZ!. 1971. Laboratory rearing of Sepiolinae (: Cephal­ in the : 30-200 m (Bello & Motolese, 1983; opoda). Marine Biology 8:82-87. Guescini & Manfrin, 1986), off Taragona: 315-363 m CADDY, J. F. 1983. The cephalopods: factors relevant to their (Sanchez & Morales, 1986), in the : 30-300 dynamics and to the assessment and management of stocks. m (Relini & Bertuletti, 1989), in the Sea of Marmara: Pp. 416-452 in J. F. Caddy (ed.), Advances in Assessment 50-140 (Katagan et al., 1993), and in the : of World Resources. FAO Fisheries Technical 86-335 (Jereb & Di Stefano, 1995). Paper, (231 ). DIGBY, B. 1949. Cephalopods from local waters at the Univer­ The presence of mature animals in every season indi­ sity of Istanbul. Nature 4141:290. cates continuous spawning throughout the year, as ob­ GABEL-DEICKERT, A. 1995. Reproductive patterns in Sepia/a af­ served by Relini & Bertuletti (1989). However, because finis and other Sepiolidae (Mollusca, Cephalopoda). Bulletin of the small number of individuals caught and the lack de l'Institut oceanographique, Monaco, Numero special 16: of samples in intermediate months, it is not possible to 73-83. define a peak or a pause of spawning. GUERRA, A. 1982. Cefal6podos capturados en la campafia "Gol­ In the ovaries of females ready to spawn, as in other fo de Cadiz-81." Resultados de Expediciones Cientfficasde! BIO Cornide, 10:17-49. cephalopods of small size (Mangold, 1987), only a frac­ GUERRA, A. 1992. Mollusca, Cephalopoda. En M.A. Ramos et tion of the total number of ova are mature at any one al. (eds.), Fauna lberica, vol. 1. Museo Nacional de Ciencias time. Therefore, fecundity estimates are misleading; one Naturales, CSIC. 327 pp. does not know the number of eggs that can mature during GUESCINI, A. & G. MANFRIN. 1986. Distribuzione di Sepiolidi a prolonged spawning period (Gabel-Deickert, 1995) nell' Adriatico centro-settentrionale. Nova Thalassia Vol. 8, The low number of eggs produced by mature females suppl. 3:513-518. may reflect a reproductive strategy also adopted by other JEREB P. & M. DI STEFANO. 1995. First observation on the Se­ piolidae (Mollusca: Cephalopoda) of the bathyal zone of the species of cephalopods (Caddy, 1983). Large yolky eggs strait of Sicily. Biologia Marina Mediterranea 2(2):205-209. under maternal protection would provide better chances KATAGAN, T., A. SALMAN, & H. AVNI BENLI. 1993. The cepha­ of survival of the young individuals than is the case in lopod fauna of the Sea of Marmara. Israel Journal of Zool­ many marine fish species. ogy 39:255-261. The maximum oocyte diameter is similar to that noted LIPINSKI, M. R. 1979. Universal maturity scale for the commer­ by Relini & Bertuletti (1989). It has to be mentioned, cially important squids (Cephalopoda: Teuthoidea). The re­ however, that some oocytes in stage III were found to sults of maturity classification of the lllex illecebrosus (LeSueur, 1821) populations for the years 1973-1977. Inter­ have smaller diameters than others in stage II, which national Commission for the NW Atlantic Fisheries Re­ means that oocytes, after the disappearance of follicular search Document 79/11/38:1-40. folds, may decrease in size. Such observations have been MANGOLD, K. 1987. Reproduction. Pp. 157-200 in P. R. Boyle made in other sepiolids too (Lefkaditou, unpublished (ed.), Cephalopod Life Cycles. Vol. II. Comparative Re­ data). In the major-axis length frequency distribution of views. eggs in the ovary and oviduct of a mature female of lllex NAEF, A. 1923. Die Cephalopoden. Fauna Flora Golf. Neapel. Monograph No 35 (Translation in English by A. Mercado, argentinus (Rodhouse & Hatfield, 1990), the largest eggs 1972.) Smithsonian Institution, Washington, D.C. 917 pp. appear in the ovary, which could also enforce this hy­ RELINI, L. 0. & M. BERTULETTI. 1989. Sepiolinae (Mollusca, pothesis. Cephalopoda) from the Ligurian Sea. Vie Millieu 39(3/4): 183-190. ACKNOWLEDGMENTS RODHOUSE P. G. & E. M. C. HATFIELD. 1990. Dynamics of growth and maturation in the cephalopod lllex argentinus de The authors wish to thank Dr. C. Papaconstantinou, head Castellanos, 1960 (Teuthoidea: Ommastrephidae). Philo­ of the research program "Assessment of Demersal Stocks sophical Transactions of the Royal Society of London, Series of Primary Importance in the Thermaikos Gulf and Thra­ B, Vol. 329:229-241. cian Sea" of the National Center for Marine Research of RUBY, G. & J. KNUDSEN. 1972. Cephalopoda from the eastern Athens (Greece), within the framework of which we col­ Mediterranean. Israel Journal of Zoology 21:83-97. lected the present material. SANCHEZ, P. & E. MORALES. 1986. Nota sobre la presencia de cuatro especies de Sepiolidae (Mollusca: Cephalopoda) en LITERATURE CITED el Mediterraneo nordoccidental espafiol. Investigaci6n Pes­ quera 50(1):137-144. BELLO, G. & G. MOTOLESE. 1983. Sepiolids from the Adriatic WIRTZ, K. 1958. Cephalopodes. Faune marine des Pyrenees­ sea (Mollusca, Cephalopoda). Rapports et proces-verbaux Orientales. Fasc 1:5-59.